Selective inhibition of NFAT activation by a peptide spanning the calcineurin targeting site of NFAT

Molecular Cell

Volumn 1, Issue 5, 1998, Pages 627-637

  Aramburu, José ^a   García Cózar, Francisco ^a   Raghavan, Anuradha ^a   Okamura, Heidi ^a   Rao, Anjana ^a   Hogan, Patrick G ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; DNA BINDING PROTEIN; DYES, REAGENTS, INDICATORS, MARKERS AND BUFFERS; GREEN FLUORESCENT PROTEIN; NFATC2 PROTEIN, HUMAN; NFATC3 PROTEIN, HUMAN; NFATC4 PROTEIN, HUMAN; NUCLEAR PROTEIN; PHOSPHOPROTEIN; PHOTOPROTEIN; SIGNAL PEPTIDE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NFAT;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CELL NUCLEUS; CHEMISTRY; ENZYMOLOGY; GENETICS; HELA CELL; HUMAN; METABOLISM; MUTAGENESIS; PHOSPHORYLATION; PHYSIOLOGY;

AMINO ACID SEQUENCE; BINDING SITES; CALCINEURIN; CELL NUCLEUS; DNA-BINDING PROTEINS; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; INDICATORS AND REAGENTS; LUMINESCENT PROTEINS; MUTAGENESIS; NFATC TRANSCRIPTION FACTORS; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN SORTING SIGNALS; TRANSCRIPTION FACTORS;

EID: 0032039075     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(00)80063-5     Document Type: Article

References (55)

1. Alessi, D.R., McDougall, L.K., Sola, M.M., Ikebe, M., and Cohen, P. (1992). The control of protein phosphatase-1 by targeting subunits. Eur. J. Biochem. 210, 1023-1035.
2. Aramburu, J., Azzoni, L., Rao, A., and Perussia, B. (1995). Activation and expression of the nuclear factors of activated T cells, NFATp and NFATc, in human natural killer cells: regulation upon CD16 ligand binding. J. Exp. Med. 182, 801-810.
3. Beals, C.R., Clipstone, N.A., Ho, S.N., and Crabtree, G.R. (1997). Nuclear localization of NF-ATc by a calcineurin-dependent, cyclosporin-sensitive intramolecular interaction. Genes Dev. 11, 824-834.
4. Bierer, B.E., Hollander, G., Fruman, D., and Burakoff, S.J. (1993). Cyclosporin A and FK506: molecular mechanisms of immunosuppression and probes for transplantation biology. Curr. Opin. Immunol. 5, 763-773.
5. Blumenthal, D.K., Takio, K., Hansen, R.S., and Krebs, E.G. (1986). Dephosphorylation of cAMP-dependent protein kinase regulatory subunit (type II) by calmodulin-dependent protein phosphatase. Determinants of substrate specificity. J. Biol. Chem. 261, 8140-8145.
6. Cameron, A.M., Nucifora, F.C.J., Fung, E.T., Livingston, D.J., Aldape, R., Ross, C.A., and Snyder, S.H. (1997). FKBP12 binds the inositol 1,4,5-triphosphate receptor at leucine-proline (1400-1401) and anchors calcineurin to this FK506-like domain. J. Biol. Chem. 272, 27582-27588.
7. 2+ flux. Cell 83, 463-472.
8. Choi, M.S., Brines, R.D., Holman, M.J., and Klaus, G.G. (1994). Induction of NF-AT in normal B lymphocytes by anti-immunoglobulin or CD40 ligand in conjunction with IL-4. Immunity 1, 179-187.
9. Coghlan, V.M., Perrino, B.A., Howard, M., Langeberg, L.K., Hicks, J.B., Gallatin, W.M., and Scott, J.D. (1995). Association of protein kinase A and protein phosphatase 2B with a common anchoring protein. Science 267, 108-111.
10. Crabtree, G.R., and Clipstone, N.A. (1994). Signal transmission between the plasma membrane and nucleus of T-lymphocytes. Annu. Rev. Biochem. 63, 1045-1083.
11. Doherty, M.J., Moorhead, G., Morrice, N., Cohen, P., and Cohen, P.T.W. (1995). Amino acid sequence and expression of the hepatic glycogen-binding GL-subunit of PP1. FEBS Lett. 375, 294-298.
12. Drewes, G., Mandelkov, E.-M., Baumann, K., Goris, J., Merlevede, W., and Mandelkov, E. (1993). Dephosphorylation of tau protein and Alzheimer paired helical filaments by calcineurin and phosphatase-2A. FEBS Lett. 336, 425-432.
13. Egloff, M.-P., Johnson, D.F., Moorhead, G., Cohen, P.T.W., Cohen, P., and Barford, D. (1997). Structural basis for the recognition of regulatory subunits by the catalytic subunit of protein phosphatase 1. EMBO J. 16, 1876-1887.
14. Endo, S., Zhou, X., Connor, J., Wang, B., and Shenolikar, S. (1996). Multiple structural elements define the specificity of recombinant human inhibitor-1 as a protein phosphatase-1 inhibitor. Biochemistry 35, 5220-5228.
15. 2+/calmodulin. J. Biol. Chem. 272, 17038-17044.
16. Griffith, J.P., Kim, J.L., Kim, E.E., Sintchak, M.D., Thomson, J.A., Fitzgibbon, M.J., Fleming, M.A., Caron, P.R., Hsiao, K., and Navia, M.A. (1995). X-ray structure of calcineurin inhibited by the immunophilin-immunosuppressant FKBP12-FK506 complex. Cell 82, 507-522.
17. Hashimoto, Y., Perrino, B.A., and Soderling, T.R. (1990). Identification of an autoinhibitory domain in calcineurin. J. Biol. Chem. 265, 1924-1927.
18. Hedin, K.E., Bell, M.P., Kalli, K.R., Huntoon, C.J., Sharp, B.M., and McKean, D.J. (1997). δ-opioid receptors expressed by Jurkat T cells enhance IL-2 secretion by increasing AP-1 complexes and activity of the NFAT/AP-1-binding promoter element. J. Immunol. 159, 5431-5440.
19. Hemmer, W., McGlone, M., and Taylor, S.S. (1997). Recombinant strategies for rapid purification of catalytic subunits of cAMP-dependent protein kinase. Anal. Biochem. 245, 115-122.
20. Hoey, T., Sun, Y.L., Williamson, K., and Xu, X. (1995). Isolation of two new members of the NF-AT gene family and functional characterization of the NF-AT proteins. Immunity 2, 461-472.
21. Hubbard, M.J., and Cohen, P. (1993). On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem. Sci. 18, 172-177.
22. Hutchinson, L.E., and McCloskey, M.A. (1995). Fc∈RI-mediated induction of nuclear factor of activated T-cells. J. Biol. Chem. 270, 16333-16338.
23. Kissinger, C.R., Parge, H.E., Knighton, D.R., Lewis, C.T., Pelletier, L.A., Tempczyk, A., Kalish, V.J., Tucker, K.D., Showalter, R.E., Moomaw, E.W., et al. (1995). Crystal structures of human calcineurin and the human FKBP12-FK506-calcineurin complex. Nature 378, 641-644.
24. Klauck, T.M., Faux, M.C., Labudda, K., Langeberg, L.K., Jaken, S., and Scott, J.D. (1996). Coordination of three signaling enzymes by AKAP79, a mammalian scaffold protein. Science 271, 1589-1592.
25. Kwon, Y.-G., Huang, H.-B., Frédéric, D., Girault, J.-A., Greengard, P., and Nairn, A.C. (1997). Characterization of the interaction between DARPP-32 and protein phosphatase 1 (PP-1): DARPP-32 peptides antagonize the interaction of PP-1 with binding proteins. Proc. Natl. Acad. Sci. USA 94, 3536-3541.
26. Lee, G., Neve, R.L., and Kosik, K.S. (1989). The microtubule binding domain of tau protein. Neuron 2, 1615-1624.
27. Liu, J. (1993). FK506 and cyclosporin, molecular probes for studying intracellular signal transduction. Immunol. Today 14, 290-295.
28. Liu, J., Farmer, J.D., Jr., Lane, W.S., Friedman, J., Weissman, I., and Schreiber, S.L. (1991). Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66, 807-815.
29. Loh, C., Carew, J.A., Kim, J., Hogan, P.G., and Rao, A. (1996a). T-cell receptor stimulation elicits an early phase of activation and a later phase of deactivation of the transcription factor NFAT1. Mol. Cell. Biol. 16, 3945-3954.
30. Loh, C., Shaw, K.T., Carew, J., Viola, J.P., Luo, C., Perrino, B.A., and Rao, A. (1996b). Calcineurin binds the transcription factor NFAT1 and reversibly regulates its activity. J. Biol. Chem. 271, 10884-10891.
31. Luo, C., Burgeon, E., Carew, J.A., McCaffrey, P.G., Badalian, T.M., Lane, W.S., Hogan, P.G., and Rao, A. (1996a). Recombinant NFAT1 (NFATp) is regulated by calcineurin in T cells and mediates transcription of several cytokine genes. Mol. Cell. Biol. 16, 3955-3966.
32. Luo, C., Burgeon, E., and Rao, A. (1996b). Mechanisms of transactivation by nuclear factor of activated T cells-1. J. Exp. Med. 184, 141-147.
33. Luo, C., Shaw, K.T., Raghavan, A., Aramburu, J., García-Cózar, F., Perrino, B.A., Hogan, P.G., and Rao, A. (1996c). Interaction of calcineurin with a domain of the transcription factor NFAT1 that controls nuclear import. Proc. Natl. Acad. Sci. USA 93, 8907-8912.
34. Lyakh, L., Ghosh, P., and Rice, N.R. (1997). Expression of NFAT-family proteins in normal human T cells. Mol. Cell. Biol. 17, 2475-2484.
35. Masuda, E., Naito, Y., Tokumitsu, H., Campbell, D., Saito, F., Hannum, C., Arai, K.-I., and Arai, N. (1995). NFATx, a novel member of the NFAT family that is expressed predominantly in the thymus. Mol. Cell. Biol. 15, 2697-2706.
36. Masuda, E.S., Liu, J., Imamura, R., Imai, S.I., Arai, K.I., and Arai, N. (1997). Control of NFATx1 nuclear translocation by a calcineurin-regulated inhibitory domain. Mol. Cell. Biol. 17, 2066-2075.
37. Mattila, P.S., Ullman, K.S., Fiering, S., Emmel, E.A., McCutcheon, M., Crabtree, G.R., and Herzenberg, L.A. (1990). The actions of cyclosporin A and FK506 suggest a novel step in the activation of T lymphocytes. EMBO J. 9, 4425-4433.
38. McCaffrey, P.G., Luo, C., Kerppola, T.K., Jain, J., Badalian, T.M., Ho, A.M., Burgeon, E., Lane, W.S., Lambert, J.N., Curran, T., et al. (1993). Isolation of the cyclosporin-sensitive T cell transcription factor NFATp. Science 262, 750-754.
39. Northrop, J.P., Ho, S.N., Chen, L., Thomas, D.J., Timmerman, L.A., Nolan, G.P., Admon, A., and Crabtree, G.R. (1994). NF-AT components define a family of transcription factors targeted in T-cell activation. Nature 369, 497-502.
40. Rao, A. (1994). NF-ATp: a transcription factor required for the coordinate induction of several cytokine genes. Immunol. Today 15, 274-281.
41. Rao, A., Luo, C., and Hogan, P.G. (1997). Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 15, 707-747.
42. Schreiber, S.L., and Crabtree, G.R. (1992). The mechanism of action of cyclosporin A and FK506. Immunol. Today 13, 136-142.
43. Shaw, K.T., Ho, A.M., Raghavan, A., Kim, J., Jain, J., Park, J., Sharma, S., Rao, A., and Hogan, P.G. (1995). Immunosuppressive drugs prevent a rapid dephosphorylation of transcription factor NFAT1 in stimulated immune cells. Proc. Natl. Acad. Sci. USA 92, 11205-11209.
44. Shibasaki, F., Price, E.R., Milan, D., and McKeon, F. (1996). Role of kinases and the phosphatase calcineurin in the nuclear shuttling of transcription factor NF-AT4. Nature 382, 370-373.
45. Shirra, M.K., Zhu, Q., Huang, H.-C., Pallas, D., and Hansen, U. (1994). One exon of the human LSF gene includes conserved regions involved in novel DNA-binding and dimerization. Mol. Cell. Biol. 14, 5076-5087.
46. Sigal, N.H., Dumont, F., Durette, P., Siekierka, J.J., Peterson, L., Rich, D.H., Dunlap, B.E., Staruch, M.J., Melino, M.R., Koprak, S.L., et al. (1991). Is cyclophilin involved in the immunosuppressive and nephrotoxic mechanism of action of cyclosporin A? J. Exp. Med. 173, 619-628.
47. Somlyo, A.P., and Somlyo, A.V. (1994). Signal transduction and regulation in smooth muscle. Nature 372, 231-236.
48. GL) subunit of glycogen-associated protein phosphatase. J. Biol. Chem. 266, 15782-15789.
49. Timerman, A.P., Wiederrecht, G., Marcy, A., and Fleischer, S. (1995). Characterization of an exchange reaction between soluble FKBP-12 and the FKBP-ryanodine receptor complex. J. Biol. Chem. 270, 2451-2459.
50. 2+ signals and immunosuppression. Nature 383, 837-840.
51. Valge-Archer, V.E., de Villiers, J., Sinskey, A.J., and Rao, A. (1990). Transformation of T lymphocytes by thev-fos oncogene. J. Immunol. 145, 4355-4364.
52. Venkataraman, L., Francis, D.A., Wang, Z., Liu, J., Rothstein, T.L., and Sen, R. (1994). Cyclosporin-A sensitive induction of NF-AT in murine B cells. Immunity 1, 189-196.
53. Wang, D.Z., McCaffrey, P.G., and Rao, A. (1995). The cyclosporin-sensitive transcription factor NFATp is expressed in several classes of cells in the immune system. Ann. NY Acad. Sci. 766, 182-194.
54. Wang, T., Li, B.-Y., Danileson, P.D., Shah, P.C., Rockwell, S., Lechleider, R.J., Martin, J., Mangarano, T., and Donahoe, P.K. (1996). The immunophilin FKBP12 functions as a common inhibitor of the TGFβ family type I receptors. Cell 86, 435-444.
55. Wesselborg, S., Fruman, D.A., Sagoo, J.K., Bierer, B.E., and Burakoff, S.J. (1996). Identification of a physical interaction between calcineurin and nuclear factor of activated T cells (NFATp). J. Biol. Chem. 271, 1274-1277.